Patterns and Processes in Plant Phylogeography in the Mediterranean Basin. A Review
Gonzalo Nieto Feliner
Real Jardín Botánico, CSIC
Plaza de Murillo 2
28014 Madrid
nieto@rjb.csic.es
Phone: +34 914203017
Mobile: +34 609446046
Running head: Plant phylogeography in the Mediterranean Basin
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Key words: glacial refugia, hybridization, latitudinal patterns, Mediterranean Basin,
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phylogeography, plants, spatio-temporal concordance, straits
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ABSTRACT
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Phylogeography, born to bridge population genetics and phylogenetics in an explicit geographic
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context, has provided a successful platform for unveiling species evolutionary histories. The
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Mediterranean Basin, one of the earth’s 25 biodiversity hotspots, is known for its complex
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geological and palaeoclimatic history. Aiming to throw light on the causes and circumstances that
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underlie such a rich biota, a review of the phylogeographic literature on plant lineages from the
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Mediterranean Basin is presented focusing on two levels. First, phylogeographic patterns are
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examined, arranged by potential driving forces such as longitude, latitude—and its interaction
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with altitude—, straits or glacial refugia. Spatial coincidences in phylogeographic splits are found
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but, in comparison to other regions such as the Alps or North America, no largely common
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phylogeographic patterns across species are found in this region. Factors contributing to
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phylogeographic complexity and scarcity of common patterns include less drastic effects of
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Pleistocene glaciations than other temperate regions, environmental heterogeneity, the blurring
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of genetic footprints via admixing over time and, for older lineages, possibly a greater
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stochasticity due to the accumulation of responses to palaeoclimatic changes. At a second level,
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processes inferred in phylogeographically-framed studies that are potential drivers of evolution
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are examined. These include gradual range expansion, vicariance, long-distance dispersal,
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radiations, hybridization and introgression, changes in reproductive system, and determinants of
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successful colonization. Future phylogeographic studies have a great potential to help explaining
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biodiversity patterns of plant groups and understanding why the Basin has come to be one of the
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biodiversity hotspots on earth. This potential is based on the crucial questions that can be
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addressed when geographic gaps are adequately filled (mainly northern Africa and the eastern
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part of the region), on the important contribution of younger lineages—for which
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phylogeographic approaches are most useful—to the whole diversity of the Basin, and on the
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integration of new methods, particularly those that allow refining the search for spatio-temporal
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concordance across genealogies.
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CONTENTS
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I. Introduction
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II. Patterns
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(1) Large-scale spatial patterns
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(a) Longitudinal patterns
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(b) Latitudinal patterns
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(c) Glacial refugia
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(d) Role of straits
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(2) Spatio-temporal phylogeographic concordance
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(3) Patterns and complexity
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III. Processes
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(a) Gradual range expansion
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(b) Vicariance
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(c) Long-distance dispersal
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(d) Radiations
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(e) Hybridization and introgression
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(f) Changes in reproductive systems
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(g) Ecology determining success of colonization
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IV. Perspectives
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V. Acknowledgements
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VI. References
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I. INTRODUCTION
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The Mediterranean Basin comprises a large territory around the Mediterranean Sea that is
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characterized by a Mediterranean climate, that is to say, mild rainy winters and hot dry summers.
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According to Quézel and Médail (2003) the Mediterranean region in a bioclimatic sense spans an
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area of 2,300,000 km2, whose limits have sometimes been suggested as coinciding with the
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natural distribution range of the olive tree (Olea europaea L.) (Fig. 1). It extends approx. 4000 km
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along an east-west axis and approx. 1600 km along a north-south axis.
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This region is of considerable biological interest because of its rich biota compared to the
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surrounding areas and is considered one of the earth’s 25 biodiversity hot-spots (Myers et al.,
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2000). At the plant species level, i.e., in floristic terms, the Mediterranean region contains a flora
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that includes c. 24.000 species of which c. 60 % are endemics (Greuter 1991) whereas, for
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instance, all of tropical Africa has a comparable plant richness (30,000 taxa) in a surface area four
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times larger (Médail and Quezel, 1997). Compared to higher latitudes, 80% of all European plant
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endemics are Mediterranean (Comes, 2004). This richness is attributed to a number of factors
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including palaeogeologic and palaeoclimatic history, ecogeographical heterogeneity, human
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influence (Blondel and Aronson, 1999; Blondel et al., 2010) and a high percentage of species with
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narrow distribution ranges (Humphries et al., 1999; Thompson, 2005).
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Geological and palaeoclimatic complexity is characteristic of the Mediterranean region. Its
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geological evolution involves complicated interactions between orogenic processes and
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widespread extensional tectonics (Rosenbaum et al., 2002). The area was formed during the
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Cenozoic simultaneously with the convergence of the African and Eurasian Plates and three
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associated smaller plates, Iberia, Apulia and Arabia (Dercourt et al., 1986; Krijgsman, 2002). The
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western Mediterranean was particularly active tectonically and consisted during the Oligocene of
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several small blocks that were remnants of a Paleozoic mountain chain, the Hercynian belt
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(Rosenbaum et al., 2002). Rotation, migration and collision processes along more than 30 Mya
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resulted in those small blocks located in the current territories of the Betic-Rif ranges, the Balearic
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Islands, the Kabylies, Corsica, Sardinia, and Calabria. The eastern Mediterranean region (Hellenic
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arc and Aegean basin) is more recent and its present configuration is the result of the collision of
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the Arabian plate with stable Eurasia in middle Miocene, which closed the connection between
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the Tethys Sea and the Indian Ocean (Krijgsman, 2002).
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The palaeoclimatic history of the Mediterranean Basin included important long-term changes
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such as the gradual global cooling since the Oligocene (Zachos et al., 2008) and an aridification
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that started c. 9-8 Mya (Van Dam, 2006). During the Late Miocene, subduction processes in the
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westernmost Mediterranean caused the closure of the marine gateways that existed between the
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Atlantic Ocean and the Mediterranean Sea, leading to the desiccation of the Mediterranean Sea
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that is known as the Messinian Salinity Crisis (MSC) 5.96-5.33 Mya (Hsü, 1972; Krijgsman, 2002).
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This period was followed by the establishment of a Mediterranean type climate, around 3.2 Mya
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(Suc, 1984). In addition, the Basin has been influenced by cyclical climatic changes, driven by the
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Milankovitch oscillations, due to periodical shifts in the Earth's orbit and axial tilt that decreased
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their periodicity to 100 Ky during the Pleistocene (Imbrie et al., 1993; Jansson and Dynesius,
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2002).
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Phylogeography has shed light on the evolutionary history of current plant species by
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bridging population genetic approaches and phylogenetic focuses, or micro- and macroevolution,
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as the father of the discipline put it (Avise et al., 1987). The geographic coverage of
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phylogeographic investigations has been more intense in regions such as North America
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(Brunsfeld et al., 2001; Soltis et al., 2006) and the Alps (Schönswetter et al., 2005), but has
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reached most regions including the Arctic (Abbott and Comes, 2004), China (Qiu et al., 2011), the
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Southern Hemisphere (Beheregaray, 2008) and also the Mediterranean region, where a
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substantial increase in the number of studies has occurred over the last ten to twelve years.
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The present paper reviews the topic of Mediterranean Plant Phylogeography aiming to throw
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light on the evolutionary history of plants in the Basin, finding clues for its biodiversity richness
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and complexity, and contributing to understand the whole puzzle of the history of European
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plants during the last 2 - 3 My. The review has a double focus, on patterns and process, and has
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been elaborated from studies published in over 130 papers.
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A summary of the knowledge concerning a very significant part of the region, i.e., the three
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southern European peninsulas (Iberia, Italy, Balkans), and the role they have played in European
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biogeography during the last million years, has been recently published (Hewitt, 2011). The
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Balkans represent the main biodiversity hotspot and the major source for postglacial colonization
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of central and northern Europe and it was suggested that such richness could be related to
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opportunities for dispersal and vicariance along a complex geological history that included several
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land connections, disconnections and submergences, particularly during the Miocene and
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Pliocene (Griffiths et al., 2004; Tzedakis, 2004). However, its geographic position closer to Asian
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biotas probably also contributed to its richness (Mansion et al., 2008).
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In the evolution of plant lineages in the Iberian Peninsula, on the other hand, determinant
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factors are the mountain ranges allowing multiple refugia and producing “a pulsating patchwork
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of allopatric to parapatric clades”, and the recurrent connections and disconnections with
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Northern Africa starting even before the MSC between 7 and 14 Mya (Hewitt, 2011).
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The Italian Peninsula is a younger conglomerate that contributed less to postglacial
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colonization of central and northern Europe due to the strong geographic barrier represented by
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the Alps. However, multiple refugia have been identified corresponding to major mountain
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blocks, with a particular differentiation in the South both in animal (e.g., Joger et al., 2007;
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Canestrelli and Nascetti, 2008) and in plant groups (Cozzolino et al., 2003; Vettori et al., 2004;
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Heuertz et al., 2006; Španiel et al., 2011).
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However, that work—one of the last by the late Godfrey Hewitt (Hewitt, 2011)—was almost
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exclusively based on studies of mammals, reptiles, amphibians and insects. Despite the common
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geological, climatic and environmental history for all organisms phylogeographic patterns might
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vary. Mechanisms such as polyploidization and hybridization, and ecogeographical concepts such
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as niche conservatism, are regarded as more significant in plants than in animal groups
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(Sanmartín, 2007; Donoghue, 2008).
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This review is focused on the species level, i.e., within species or closely-related species, as
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was the original scope of Phylogeography (Avise et al., 1987). However, there is not a sharp
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border line between species and closely-related species and thus some works going beyond the
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species level that were important for the Mediterranean Basin have also been considered. On a
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geographic side, despite being traditionally considered a part or an extension of the
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Mediterranean region, the Macaronesian archipelagos have not been considered here because
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oceanic island biogeography (and phylogeography) is a specific field that has received much
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attention in recent years and a considerable part of the literature has been devoted to the
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Macaronesian region (Juan et al., 2000; Sanmartín et al., 2008; Fernández-Palacios et al., 2011).
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II. PATTERNS
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In this section, the main phylogeographic patterns detected in plant groups across the
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Mediterranean Basin are arranged following the inferred major driving forces or causal factors.
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(1) Large-scale spatial patterns
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Even if small scale factors and specific biological properties of the plant groups are important in
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driving differentiation in an environmentally heterogeneous region like this, large scale factors
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also have a role in contributing to gene flow interruption, and thus to phylogeographic splits. The
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patterns listed below (longitudinal, latitudinal, sea straits, refugia) are associated to longitude and
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latitude, spanning the size and shape of the region, and potentially contributed to create shared
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patterns across plant groups.
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(a) Longitudinal patterns
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East-west phylogeographical breaks, i.e, occurring along the longest axis of the Mediterranean
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Basin, have frequently been inferred, and sometimes dated, to have arisen as a consequence of
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pre-Pleistocene diversification of lineages. The most apparent cases are those in which there is a
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clear current geographical gap associated with a phylogeographic split, which might have resulted
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from contraction of formerly continuous ranges. These disjunctions or highly scattered ranges are
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seen in the lowland shrub Buxus balearica Lam. (Rosselló et al., 2007; Fig. 2), the salt-tolerant
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succulent Microcnemum coralloides (Loscos & J. Pardo) Buen (Kadereit and Yaprak, 2008) or the
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herbaceous legume Erophaca baetica (L.) Boiss. from evergreen oak forests (Casimiro-Soriguer et
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al., 2010). In the coastal subshrub Cephalaria squamiflora (Sieber) Greuter such gap is emphasized
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by its insular distribution ranging from the Balearics to the Aegean (Rosselló et al., 2009). When
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there is no current geographic gap, the location of the phylogeographic break or the secondary
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contact may still be detectable (e.g., in the perennial mountain herb Heliosperma pusillum
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(Waldst. & Kit.) Rchb., Frajman and Oxelman, 2007), particularly when the distribution range is
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linear as in the marsh sedge Carex extensa Gooden. (Escudero et al., 2010). It is however more
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frequent that events subsequent to the initial gene flow interruption, such as partial westwards
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colonization of genotypes originated in the East or vice versa, led to a more complex picture, as in
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the case of the submediterranean herbaceous Anthyllis montana L. (Kropf et al., 2002), the laurel
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trees Laurus nobilis L. and L. azorica (Seub.) Franco (Rodríguez-Sánchez et al., 2009) or the
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thermophilous lowland shrub Myrtus communis L. (Migliore et al., 2012). Westward or eastward
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waves of colonization, not only during the Pleistocene but at different times depending on the
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climatic conditions and the ecological requirements of the species in question, have been decisive
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in shaping the current species and genetic composition of the Mediterranean flora. Examples are
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found in Araceae, Carex extensa, Erica arborea L. or Myrtus communis (Mansion et al., 2008;
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Escudero et al., 2010; Désamoré et al., 2011; Migliore et al., 2012; respectively). Such expansions
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have been reported to be important during the Oligocene–Miocene, when microplates located
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between Paratethys and Tethys allowed land connections along the Mediterranean (Steininger
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and Rögl, 1984; Meulenkamp and Sissingh, 2003). However, other organisms expanded through
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the Southern rim of the Basin at different periods (North Africa – Arabia, Quézel, 1985) as the
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steppic herbaceous perennial Ferula loscosii (Willk.) Lange (Pérez-Collazos et al., 2009) or some
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thistles (Cardueae; Barres et al., 2013).
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In addition to east-west phylogeographic splits, different levels in genetic diversity on a large
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scale in eastern vs. western areas of the Mediterranean Basin have been found too, particularly in
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trees. Some of those E-W differences have been related to the place of origin or major
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diversification of the group in question (e.g., in Quercus suber L., Lumaret et al., 2005), while for
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other groups decisive factors have occurred along their evolutionary history. For instance, among
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gymnosperm tree species from the genus Abies, Cedrus, Cupressus and Pinus, a decreasing trend
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in genetic diversity running east-west along the Basin has been detected and has been attributed
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to an east (warm/wet) – west (cold/dry) trend during the last glacial maximum (LGM) (Fady, 2005;
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Wu et al., 2007). Such a decreasing gradient of within-population genetic diversity from east to
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west has also been found in a meta-analysis based on different groups of living organisms, but it is
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stronger in the southern part (northern Africa) than in the northern Mediterranean, in low-land
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plants than in plants at higher elevations, in trees that in other life-forms, and in bi-parentally and
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paternally than in maternally inherited DNA markers (Conord et al., 2012). However, there is no
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overall correlation between genetic diversity and species diversity across the Basin (Fady and
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Conord, 2010) and different situations concerning richer eastern or western lineages are found at
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the species level (e.g., in Cistus, Guzmán and Vargas, 2005; Hordeum, Jakob et al., 2007; or
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Heliosperma, Frajman and Oxelman, 2007). Therefore, new evidence is necessary to understand
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the extent and causes for the prevailing idea that the Eastern Mediterranean is a reservoir for
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plant evolution or a cradle for lineages diversification (Mansion et al., 2009; Roquet et al., 2009;
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Barres et al., 2013).
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(b) Latitudinal patterns
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As at the global scale from the poles to the Equator, diversity patterns associated with latitude are
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also found in the Mediterranean region. The pattern that is most directly associated to latitude is
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a north-south decreasing genetic diversity gradient occurring within lineages. This applies mainly
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to the northern Mediterranean region and is even more explicit when territories north of the
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Region are also considered. It resulted from the ways by which species responded to the climatic
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oscillations during the Pleistocene searching for their climatic optimum, i.e., shifting their ranges
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northwards or southwards. For cold-sensitive species this implied that a significant portion of
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diversity lost in northern latitudes during glacial periods was preserved in southern regions and
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also that only part of the genotypes, usually those occurring on the northern edge or closest to
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the glaciated areas, recolonized the northern territories during the Interglacials (Hewitt, 2000).
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Such south-north recolonization processes were rapid and resulted in a few genotypes occupying
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much larger areas in northern latitudes in Europe compared to Mediterranean territories as well
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as in a few alleles surfing on the front of the colonizing populations (Excoffier and Ray, 2008).
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This—so called leading-edge expansion model—has been used to explain genetic diversity
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gradients within lineages that are likely to have been due to sequential bottlenecks during
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colonization of deglaciated areas. Contrasting roles in leading vs. trailing-edge populations led to
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differential patterns in gene flow, differentiation and ultimately in shaping the genetic diversity of
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the species (Hampe and Petit, 2005; Parisod and Joost, 2010).
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The scenario of climatically-driven north-to-south range shifts took place in highly
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mountainous terrain in many areas of the Basin particularly in Southern Europe, which
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contributed to shape latitudinal patterns beyond a plain latitudinal diversity gradient. One of the
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simplest approaches to focus on this latitude-altitude interaction was Kropf et al.’s (2006; 2008)
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“successive vicariance” model regarding the postglacial retreat of cold-adapted species into high
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elevations. They tested the implications of the assumption that the retreat should progress in
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Europe from south to north as interglacial periods became warmer (De Beaulieu et al., 1994). On
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the Iberian Peninsula, such a model would result in greater genetic distance between populations
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from Sierra Nevada and the Pyrenees than between the Pyrenees and the Alps because the
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southernmost populations had to retreat—and thus interrupt gene flow—earlier. They found
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results consistent with this prediction in some, e.g., Silene rupestris L., Kernera saxatilis (L.) Rchb.,
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Gentiana alpina Vill. and Saxifraga oppositifolia L., but not all species studied (Kropf et al., 2006;
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2008).
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(c) Glacial refugia
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Mountains provided another dimension, altitude, to the latitudinal gradient and contributed
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to compartmentalize the region creating climatically suitable enclaves, which allowed glacial
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refugia to occur. According to Médail and Diadema (2009), refugia are areas “where distinct
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genetic lineages have persisted through a series of Tertiary or Quaternary climate fluctuations
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owing to special, buffering environmental characteristics”. Glacial refugia have important
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biological implications, e.g., for conservation under a climate change scenario (Tzedakis, 2004).
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The well-known general pattern of refugia in areas less affected by glaciations is strongly
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supported by the fossil data (Bennet et al., 1991) and phylogeographic studies have made a major
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contribution to identifying them (e.g., Taberlet et al., 1998; Hampe et al., 2003; Heuertz et al.,
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2004; Provan and Bennett, 2008). But there have been different views on the number of refugia in
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each species. Hewitt (2001) proposed the ‘paradigm postglacial colonization patterns’ model,
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which considered each of the main sources of recolonization for northern European territories,
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i.e., the three Mediterranean peninsulas (Iberian, Italian and Balkan), as a single refugium.
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Although this scheme was useful for tree species in particular (Taberlet et al., 1998; Heuertz et al.,
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2004), it was too simple to account for the evolutionary history of many groups due to the
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importance of orography, among other factors. The ‘refugia-within-refugia’ model proposed by
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Gómez and Lunt (2007) as a response to the latter advocates that phylogeographic breaks within
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these peninsulas in a number of animal and plant groups demonstrate the preservation of various
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lineages and thus the occurrence of multiple refugia. In fact, in those phylogeographic studies
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that include Mediterranean populations together with populations from elsewhere, the
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occurrence of multiple refugia in one or more of the three Peninsulas is the norm both for
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herbaceous (Picó et al., 2008) and tree species such as Quercus spp. (Olalde et al., 2002; López de
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Heredia et al., 2007), Populus spp. (Macaya-Sanz et al., 2012) or other groups (Carrión et al., 2003;
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reviewed for Iberia in Rodríguez-Sánchez et al., 2010). Although there are more phylogeographic
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examples from the Iberian Peninsula the refugia within refugia model clearly holds for the Italian
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(Cozzolino et al., 2003; Ansell et al., 2008; Grassi et al., 2009; Španiel et al., 2011) and Balkan
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peninsulas (Heuertz et al., 2001; Trewick et al., 2002; Kučera et al., 2010; Surina et al., 2011) (Fig.
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3). This multiple refugia pattern has also been inferred in Southern Australia (Byrne, 2008),
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probably because as in the Mediterranean Basin effects of climatic oscillations allowed survival
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and resilience of different partly or totally isolated lineages within larger territories.
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Spatial coincidence of refugia for different species greatly increases their interest as a sort of
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sanctuaries for plant diversity (Tribsch and Schönswetter, 2003). There is coincidence at relatively
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gross scales, e.g., the Andalusian ranges, Sicily or the Aegean region. However, factors related to
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the biology or history of the group in question hinder fine matches for the location of refugia
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across groups. For instance, there are scenarios that include also non-Mediterranean refugia, e.g.,
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in Meconopsis cambrica (L.) Vig. (Valtueña et al., 2012) or specific traits associated with the
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location of refugia, e.g., higher clonality in northern populations of Populus, more exposed to
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glaciations (Macaya-Sanz et al., 2012). Another feature that has been found in Fagus and other
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trees is the unexpectedly high degree of genetic diversity detected in non-Mediterranean
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latitudes away from the glacial refugia even if allelic diversity was higher in the latter (Comps et
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al., 2001; Widmer and Lexer, 2001; Petit et al., 2003). This pattern is due to the admixture of
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divergent lineages recolonizing the continent from separate refugia.
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In a previous paper I argued that evidencing refugia, even for refugia within refugia, was not an
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ultimate goal but a first step in phylogeographic studies in the Mediterranean Basin (Nieto Feliner,
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2011) because as sites where extinction has been minimized, the processes that underlie survival
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in them seem to be of primary interest. Also, in the context of the scarcity of phylogeographic
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patterns in the Mediterranean Basin (see patterns and complexity section), refugia represent an
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exception and demand for explanatory processes. In the end—simple as it might sound—refugia
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might be environmentally favorable enclaves in spatially convenient sites. This is consistent with a
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long series of studies in the Alps (Schönswetter et al., 2005) and particularly with the finding of a
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coincidental current genetic structure across numerous taxonomic plant groups that is correlated
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with specific substrata (Alvarez et al., 2009). It seems that cases like this exemplify a meaningful
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integration of historical and ecological components of biogeography that allows a better
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understanding of current distribution patterns. Along this line, glacial refugia represent interesting
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places from the community ecology perspective (Webb et al., 2002). As enclaves where
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conservation is maximized and at the same time have a biogeographic dynamic nature, examining
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phylogenetic community structure along with concepts such as habitat filtering vs. competitive
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exclusion of closely related species can help understand the functioning of refugia.
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(d) Role of straits
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It is likely that straits have been an important modulator of phylogeography across the region (Fig.
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4). This role is not unexpected in a region whose coastline stretches 46,000 km, making the sea a
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barrier for biological exchange not only between islands but also between mainland and islands or
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between mainland areas. The effectiveness of the sea as a barrier has varied over time due to
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climatic and geological changes and depending on the plant group. For example, one of the most
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significant sea barriers geographically, the Strait of Gibraltar, is considered to be a greater
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biogeographic barrier than the Pyrenees or the Alps (Hewitt, 2011) and has acted as such for
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species such as the continental juniper Juniperus thurifera L. (Terrab et al., 2008b), a sedge
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growing in Quercus suber forests Carex helodes Link (Escudero et al., 2008), Abies spp. (Terrab et
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al., 2007) or several Mediterranean conifers (Jaramillo-Correa et al., 2010), among others.
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However, a number of studies found that it was not effective at interrupting gene flow between
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African and European populations in both directions, e.g., in the bulbous monocot Androcymbium
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gramineum (Cav.) McBride (Caujapé-Castells and Jansen, 2003), the coastal annual Hypochaeris
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salzmanniana DC. (Ortiz et al., 2007), the legume shrub Calicotome villosa (Poir.) Link (Arroyo et
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al., 2008), several mediterranean rockroses Cistus spp. (Guzmán and Vargas, 2009; Fernández-
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Mazuecos and Vargas, 2010) or in Rosmarinus officinalis L. (Mateu et al., 2013). This variable role
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of the strait of Gibraltar depending on the species is consistent with results from animal groups
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(Hewitt, 2011). The lack of correlation between dispersal abilities and genetic exchange between
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the two continents across this Strait is also noteworthy (Rodríguez-Sánchez et al., 2008; Guzmán
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and Vargas, 2009).
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The geographic position of straits, and not only their width, is a crucial factor in determining
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their biogeographic role. For instance, besides filtering biological exchange between Africa and
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Europe, the Strait of Gibraltar has been decisive in shaping diversity patterns in the area. The
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concentration of plant diversity on both sides of the Strait, due to both the accumulation of relict
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species and the high percentage of endemics, is likely to be strongly related to its geographic
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location as a crossroad, which allows it to act as a melting-pot for lineages (Rodríguez-Sánchez et
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al., 2008).
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The depth of seafloor is another important factor since shallow waters maximized the effects
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of eustatic sea-level shifts by narrowing the straits, modifying the shape and size of emerged
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lands or even creating land corridors. Along the Mediterranean Basin, the MSC has been widely
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classically invoked as the fundamental cause for land connections involving relatively shallow sea
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floors (Bocquet et al., 1978) and, more moderately, after the advent of molecular data (e.g., in
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Androcymbium gramineum for Gibraltar, Caujapé-Castells and Jansen, 2003; in the orchid
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Anacamptis palustris (Jacq.) R.M. Bateman et al., for the Otranto Strait, Mussacchio et al., 2006).
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In contrast to the MSC, the phylogeographic importance of Pleistocene land-bridges has not
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been adequately considered until recently, when dated genealogical splits have been associated
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to sea-level drops of up to 130 m that occurred during the LGM (Petit et al., 2002; Lambeck et al.,
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2002). For instance, the current relationships between species across the Sicilian Channel were
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shaped by eustatic sea-level shifts during the Pleistocene that facilitated biotic exchange between
334
Sicily and Tunisia and also between the islands in the region, Malta, Pantelleria, Lampedusa, and
335
the Aeolian and Aegadian archipelagos (Naciri et al., 2010; Zitari et al., 2011; Lo Presti and
336
Oberprieler, 2011; Fernández-Mazuecos and Vargas, 2011). In the Balearic Islands marine
337
transgressions during the interglacial periods divided the island of Majorca into two, whereas
338
during marine regressions sea-level drops united Majorca, Menorca and Cabrera into a single land
339
mass (Vesica et al., 2000; Gràcia et al., 2001). The latter regression during the Upper Pleistocene
340
at the end of the Mindel glaciation (c. 400,000 y BP) also connected Ibiza with the Dianic range in
341
Iberia which allowed biotic exchanges, e.g., in the perennial herb Cheirolophus intybaceus (Lam.)
342
Dostál (Garnatje et al., 2013). These eustatic sea-level shifts subsequently promoted or restricted
343
intraspecific gene flow, fragmenting populations and enhancing their divergence, e.g. in two
344
Asteraceae herbaceous Balearic endemics such as Senecio rodriguezii Willk. ex J.J. Rodr. (Molins et
345
al., 2009) and Crepis triasii (Cambess.) Nyman (Mayol et al., 2012). The impact of Pleistocene land-
346
bridges is also detectable in the Aegean sea (Bittkau and Comes, 2005) and is evident in narrow
347
and shallow straits like Bonifacio, between Corsica and Sardinia, which are not associated with
348
any phylogeographic break in a plastid haplotype network of the rockrose Cistus creticus L. (Falchi
349
et al., 2009).
350
The biology of the plants can result in opposite effects of the same strait on different species.
351
For instance, in the Eastern Mediterranean, phylogeographic breaks have been detected
352
coinciding with the straits of Bosporus for two species from sandy beaches such as Eryngium
353
maritimum L. and Cakile maritima Scop., and with the Dardanelles for Cakile maritima (Kadereit
354
and Westberg, 2007). However, because these two species occur in coastal habitats, Bosporus
15
355
and Dardanelles acted as geographic barriers in opposite periods compared to inland plants, and
356
along different geographic orientations (roughly east-west instead of north-south). Thus, unlike
357
for inland species, the closure of the two straits that resulted in the isolation of the Black Sea, the
358
Sea of Marmara and the Aegean Sea could represent an east-west barrier for a coastal expansion
359
of these species due to elimination of coastline. Yet, on the other end of the Basin, the fact that
360
the Strait of Gibraltar has remained open since the end of the MSC (c. 5.3 Mya) did not imply that
361
coastal land plants species could spread freely across it along an east-west direction; this was
362
probably due to sea-currents that precluded gene-flow via seeds in species with sea-dispersed
363
fruits (Kadereit and Westberg, 2007; Westberg and Kadereit, 2009). Sea-currents have been also
364
invoked to explain limitations to gene flow across the same strait for marine species (reviewed in
365
Patarnello et al., 2007). In all, the conclusion is that predicting the role of straits as
366
biogeographical barriers requires considering very diverse factors.
367
368
(2) Spatio-temporal phylogeographic concordance
369
Genealogical concordance is the most straightforward evidence for common historical factors
370
affecting the phylogeography of different groups in the Mediterranean region. Different types of
371
concordance are conceivable and Avise (1998; 2009) pointed out four: within-locus, multi-locus,
372
multi-species and among multiple lines of empirical evidence. The third of these—geographical
373
co-location of significant genealogical splits across multiple co-distributed species—has been
374
addressed using comparative phylogeographic approaches (Bermingham and Moritz, 1998) in the
375
Alps (e.g., Tribsch and Schönswetter, 2003; Schönswetter et al., 2004) or North America
376
(Brunsfeld et al., 2001; Soltis et al., 2006). In the Mediterranean Basin some comparative studies
377
have focused on taxonomic groups such as Cistus spp. (Fernández-Mazuecos and Vargas, 2010),
378
exemplifying how different phylogeographic patterns can arise in closely related species. Other
379
studies have focused on phylogenetically unrelated plants from similar habitats. In alpine
16
380
Mediterranean plants no common pattern was found (Vargas, 2003) whereas in coastal
381
communities there was some concordance in geographic clusters in the Eastern Mediterranean
382
but no strongly congruent patterns along their inferred evolutionary histories (e.g., Kadereit et al.,
383
2005; Kadereit and Westberg, 2007). The conclusion that species sharing habitats and even
384
showing co-located phylogeographic breaks might not share much of their overall
385
phylogeography is consistent with results from the early comparative study on the continental
386
scale by Taberlet et al. (1998).
387
In fact, co-location of phylogeographic breaks in different groups does not always imply time
388
or process coincidence, a phenomenon recognized as pseudocongruence at a deeper
389
biogeographic level (Donoghue and Moore, 2003). Pseudocongruence at the species level has
390
recently been shown by Jaramillo-Correa et al. (2010) in a study of five species of Mediterranean
391
conifers across the Strait of Gibraltar. And this concept is also applicable to the similarities in
392
ecological requirements of the species that coincide in Alpian refugia, commented above (Alvarez
393
et al., 2009). Also, evolutionary patterns need not be associated with important climatic events,
394
as illustrated by the diversification rates in the annual self-compatible Nigella arvensis L. group,
395
which were not affected by the onset of the Mediterranean climate (Bittkau and Comes, 2009).
396
Another commonly followed search for concordance examines matches between gene-tree
397
partitions (or historical patterns in general) of a given study group and dated historical abiotic
398
events (geographic or climatic changes). For instance, hybridization and introgression between
399
previously lineages can be associated to a breakdown of existing geographic barriers. Although
400
searches for this type of concordance are frequently hampered by too wide confidence intervals
401
for estimated dates of lineage events (Fromhage et al., 2004), a number of studies using dated
402
phylogeographies have proposed association between climatic or geographic factors and
403
evolutionary events in the Mediterranean (e.g., in Anthemis, Lo Presti and Oberprieler, 2009;
404
Dianthus, Valente et al., 2010; Erodium, Fiz-Palacios et al., 2010). Still, difference in coalescence
17
405
times should ideally be taken into account when examining matches of evolutionary patterns in
406
different species with the same abiotic event (see Perspectives section).
407
Lack of phylogeographic structure associated to rapid postglacial colonization also results in
408
some form of concordance. This seems to be the case in two tree species which, together with
409
long generation times, share the possession of edible fruits, which might have accelerated their
410
colonization of the Basin by humans: the stone pine, Pinus pinea L. (Vendramin et al., 2008) and
411
the chestnut tree, Castanea sativa Miller (Fineschi et al., 2000).
412
413
(3) Patterns and complexity
414
The main conclusion from the available evidence is that common phylogeographic patterns are
415
scarce in the Mediterranean Basin. In the Alps phylogeography has focused on postglacial
416
colonization, testing whether refugial areas could have existed in nunataks or at lower latitudes
417
(e.g., Tribsch and Schönswetter 2003; Schönswetter et al. 2005). The distinct patterns found in
418
this region seem to result from younger histories, whereas previous lineages disappeared due to
419
Pleistocene glaciations.
420
Compared to the Alps, scarcity of patterns in the Mediterranean Basin may partly derive from
421
blurring of genetic footprints via admixing over time. The successive contacts between
422
populations that have experienced some differentiation during glacial or interglacial periods, but
423
failed to develop complete reproductive barriers, lead to admixture and thus obscured genetic
424
footprints of whatever differentiation might have preceded those contacts. Scarcity of common
425
patterns may actually reflect a scarcity of simple patterns and thus be related to the idea of
426
complexity. In the Mediterranean Basin several phylogeographic studies have highlighted this
427
(Heuertz et al., 2004; Jiménez et al., 2004; López de Heredia et al., 2005, 2007; Médail and
428
Diadema, 2009; Lo Presti and Oberprieler, 2011; Fernández-Mazuecos and Vargas, 2011).
429
However, species of older, Tertiary, origin such as Erica arborea (Désamoré et al., 2011) or Myrtus
18
430
communis (Migliore et al., 2012) exemplify the idea of complexity resulting from survival and
431
partial admixture of lineages. These studies report a combination of extensive colonization waves
432
(frequently east-west or vice versa) and survival without great geographic displacement or, as
433
expressed in Migliore et al. (2012) “accumulation of the species’ responses to successive
434
palaeoenvironmental changes”. Also for older lineages, such accumulation of responses under
435
substantial climatic instability but without dramatic unifying climatic changes probably resulted in
436
greater stochasticity, which contributed to the scarcity of phylogeographic patterns in the Basin.
437
438
III. PROCESSES
439
Although comparative studies in the Basin have primarily looked for common patterns the
440
possibility of inferring common processes from different groups would be a great advantage
441
albeit a challenging one. The coincidence in space of the same processes in different species
442
poses the question of whether similar selection pressures lie behind them. Some of the processes
443
can be addressed within the frame of statistical phylogeography approaches that estimate
444
population parameters (Hickerson et al., 2010) but the focus here is wider. The following
445
paragraphs highlight a few processes that have been inferred, from phylogeographically-framed
446
studies, to occur in Mediterranean lineages and may be drivers, or at least important factors, in
447
the evolutionary history of plant groups. These are gradual range expansion, vicariance, long-
448
distance dispersal (LDD), radiations, hybridization and introgression, changes in reproductive
449
systems, and ecological determinants of colonization. The first three of those specifically refer to
450
changes in species distributions while the remaining are primarily involved in other aspects of
451
evolutionary change, such as shaping species genetic architecture, although ultimately affect their
452
distributions too. All of them have implications on phylogeography although in different ways and
453
at different time scales.
454
19
455
(a) Gradual range expansion
456
Following from the simplest way by which plants, as sessile organisms, track their climatic optima
457
during climate changes it is likely that gradual range expansion has played an important role, if
458
not the most, in distribution range changes over time. Such expansion has mainly occurred along
459
a north-south direction and along elevational gradients in the mountains and is currently
460
detectable, even at minimal time-scales, in alpine pioneer species as a response to global change
461
(Pauli et al., 2007). But other gradual range expansion scenarios not evidently driven by rapid
462
climate changes might have been also common in the Mediterranean. Gradual expansion should
463
have contributed substantially to westwards or eastwards colonization along the Basin either
464
across the northern (European) side or across Northern Africa and might account for small-scale
465
migration as reported in Anthyllis montana (Kropf et al., 2002).
466
(b) Vicariance
467
Mediterranean phylogeographic studies sometimes set as the null hypothesis the possibility that
468
current disjunct distributions of genotypes, species or closely related species are due to
469
vicariance, that is, the fragmentation of an ancient continuous range. The oldest tectonic events
470
invoked to explain currently recognizable patterns in this region date back to the geological
471
dynamism in the Oligocene that led to isolation of previously connected land-masses (Rosenbaum
472
et al., 2002). Thus, lineage splits in herbaceous lineages attributed to vicariance during that
473
period do not involve populations within species but closely related genera such as Helicodiceros
474
and its Eastern Mediterranean sister group Eminium (Mansion et al., 2008). However, in slowly
475
evolving tree species the idea that current genetic structures may reflect population divergence
476
pre-dating the onset of the Mediterranean climate (c. 3.2 Mya) is not perceived as odd (Petit et
477
al., 2005). Particularly striking is the interpretation of the partial matching found in Quercus suber
478
between current plastid intraspecific lineages and the western European Oligocene microplates,
20
479
which was attributed to tectonic-associated vicariance events produced at that time (Magri et al.,
480
2007).
481
The complex palaeogeology and palaeoclimatology of the Basin counteracted vicariance by
482
favoring contacts between previously isolated land-masses and the migration of island arcs. The
483
outcome is a reticulate biogeographical history in which ‘biotas repeatedly fragmented and
484
merged as dispersal barriers appeared and disappeared through time’ (Sanmartín, 2003; Salvo et
485
al., 2010). Therefore, finding whole matches between several areas and genetic groups is an
486
exception and the most frequent pattern is matches in single vicariant events separating two
487
lineages. Examples of this include both woody species such as Myrtus (Migliore et al., 2012) and
488
non-woody species such as Campanula (Cano-Maqueda et al., 2008), some of them associated
489
with well-dated raising of barriers, e.g., the opening of the Strait of Gibraltar, 5.3 Mya, in
490
Anthemis (Lo Presti and Oberprieler, 2009) or Linaria (Fernández-Mazuecos and Vargas, 2011).
491
A more recently reported model of vicariant relationship is associated with Pleistocene
492
climatic oscillations. During interglacial periods (including the current ‘postglacial’ one),
493
distribution areas of cold-adapted species were fragmented and restricted to higher elevations,
494
thus creating vicariance, which may have left genetic footprints. Current patterns attributed to
495
this type of vicariance have been reported in high elevation species, both herbaceous perennials
496
such as Pritzelago alpina (L.) Kuntze (Kropf et al., 2003), Silene rupestris, Gentiana alpina, Kernera
497
saxatilis, Saxifraga oppositifolia (Kropf et al., 2006; 2008), Androsace vitaliana (L.) Lapeyr. (Dixon
498
et al., 2009), Reseda sect. Glaucoreseda (Martín-Bravo et al., 2010) as well as trees such as Pinus
499
mugo Turra (Heuertz et al., 2010).
500
(c) Long-distance dispersal
501
LDD events inferred in the frame of phylogenetic studies of genera or species groups, using
502
analytical methods, have not been rare within the Mediterranean region (e.g., in Araceae,
503
Mansion et al., 2009; Erodium, Fiz-Palacios et al., 2010) and between this and other regions (e.g.
21
504
in Senecio, Coleman et al., 2003; Convolvulus, Carine et al., 2004; Hypochaeris, Tremetsberger et
505
al., 2005; Oligomeris, Martín-Bravo et al., 2009; Legousia, Roquet et al., 2009; and other groups,
506
Kadereit and Baldwin, 2012). At the phylogeographic level, the sharper the contrast between
507
genetic and geographic distance (specifically a low genetic distance combined with a high
508
geographic distance) the clearer the footprint of the LDD event is, which implies that older LDD
509
events are more difficult to document. LDD has been suggested to occur between mountain
510
ranges affecting cold-tolerant plants only recently, e.g., Alps and Iberian ranges (Androsace
511
vitaliana, Dixon et al., 2009), Pyrenees and Sierra Nevada (Papaver alpinum L., Kropf et al., 2006).
512
This is perhaps in contrast to those events mediated by marine bird flights involving coastal or low
513
elevation species, which have been considered classical examples of LDD. Of those LDD events
514
connecting areas isolated by sea, there are a number of reports between the Iberian Peninsula
515
and the Balearics (e.g., Cheirolophus intybaceus, Garnatje et al., 2013), the Iberian Peninsula and
516
Corsica-Sardinia (Armeria pungens (Link) Hoffmanns. & Link, Piñeiro et al., 2007; Juniperus
517
thurifera, Terrab et al., 2008b), as well as across the Strait of Sicily (Anthemis secundirramea Biv.,
518
Lo Presti and Oberprieler, 2011; Linaria Sect. Versicolores, Fernández-Mazuecos and Vargas, 2011)
519
(Fig. 5). For other coastal plants, marine long-distance dispersal has been important in some
520
species (e.g. Calystegia soldanella (L.) R. Br., Arafeh and Kadereit, 2006).
521
(d) Radiations
522
Although adaptive radiations are usually associated to islands (e.g., Aeonium in the Canary Islands,
523
Jorgensen and Ollesen, 2001), correlations between morphological traits and environmental
524
variables have revealed cases in the Mediterranean Basin, e.g., in Cistus (Guzmán et al., 2009).
525
Perhaps this is not unexpected given the environmental heterogeneity of the Basin and the
526
patchy landscape that offer a variety of niches in relatively close proximity. However, in some
527
cases there is no evidence for considering the radiations to be adaptive, e.g., in Dianthus broteri
528
Boiss. & Reuter (Balao et al., 2010) and Erodium spp. (Fiz-Palacios et al., 2010), while in others
529
radiations are explicitly considered non-adaptive. In fact, comparatively buffered climatic
22
530
oscillations and relatively uniform environments in the Aegean region have favored non-adaptive
531
radiation, driven instead by genetic drift and leading to allopatric speciation in this area, e.g., in
532
the Nigella arvensis group (Bittkau and Comes, 2005; Comes et al., 2008). Studies on other groups
533
are consistent with a scenario of random drift as the driver of plant diversification in the Aegean
534
region (e.g., Brassica cretica Lam., Edh et al., 2007). Altogether, these examples have stressed the
535
importance of non-adaptive radiation as compared to the most extended model of radiative
536
evolution (Gittenberger, 1991).
537
(e) Hybridization and introgression
538
The Mediterranean Basin gathers historical and ecological factors that render it a fertile arena for
539
hybridization and introgression (Thompson, 2005). Firstly, it is a biodiversity hotspot containing a
540
high degree of genetic and species diversity accumulated in a comparative small space over
541
extended time (Médail and Diadema, 2009). Secondly, adequate conditions have existed to
542
encourage contact between partially differentiated populations and closely related species.
543
Quaternary climate-driven shifts in species ranges involved shorter distances than in higher
544
latitudes (Hewitt, 2001) in part due to the fact that orography enabled species to track their
545
niches along altitude (Gutiérrez Larena et al., 2002; Naciri et al., 2010; Fuertes Aguilar et al., 2011;
546
Surina et al., 2011). This, together with the patchy nature of the landscape and the narrow ranges
547
of many species (Thompson, 2005) contributed to those contacts. There is evidence that contact
548
zones between close species of Antirrhinum that are able to hybridize can be finely defined by
549
niche modelling (Khimoun et al., 2012). This gives ground to the idea that maximizing ecotones in
550
a patchy landscape can favor hybridization in the Mediterranean and is also consistent with the
551
importance of ecological differentiation in the region (Thompson et al., 2005). Another favorable
552
environmental circumstance is habitat disturbance (Lamont et al., 2003; Seehausen et al., 2008)
553
and domestication, usually progressing from east to west (Besnard et al., 2007; 2013). In
554
comparison to central or northern European regions, humans have substantially altered the
555
Mediterranean Basin landscape over several thousand years, both through cultivation and
23
556
habitation, as well as by introducing non-native species. Disturbed habitats provide a suitable
557
ground for hybridization (Anderson, 1948; Levin et al., 1996) and the potential of alien species to
558
become invasive has been associated to hybridization too (Schierenbeck and Ellstrand, 2009).
559
These factors suggest that hybridization and introgression, which are common features in
560
plants throughout the world, might have been quantitatively important in the Mediterranean.
561
Testing if this is true is important because these processes can be main drivers of plant evolution
562
(Arnold, 1997; Mallet, 2005) but by no means easy because there are different possible
563
evolutionary outcomes of hybridization and introgression (Arnold, 1997; Soltis and Soltis, 2009)
564
that require specific pattern-detection strategies. Despite these difficulties, hybridization and
565
introgression have been detected in the Region based on different patterns. These include
566
incongruence between differently inherited markers (in Centaurium, Mansion et al., 2005;
567
Helliosperma, Frajman and Oxelman, 2007; Olea, Besnard et al., 2007; Anthemis, Lo Presti and
568
Oberprieler, 2011); sharing of haplotypes (e.g., in evergreen oaks, Belahbib et al., 2001; López de
569
Heredia et al., 2007; and Fraxinus, Heuertz et al., 2006) sometimes linked to altitudinal shifts (in
570
Armeria, Gutiérrez Larena et al., 2002); quantitative morphological variation, especially
571
intermediacy (in Cyclamen; Thompson et al., 2010); coalescent simulations to tell apart
572
hybridization from incomplete lineage sorting (in Linaria, Blanco-Pastor et al., 2012); or, more
573
rarely, species-independent geographic structure of variation for nuclear ribosomal DNA ITS (in
574
Armeria, Nieto Feliner et al., 2004).
575
Three aspects remain crucial to refine the assessment of the true incidence of
576
hybridization and introgression in the region. Understanding and documenting the ecological
577
factors, and in particular the adaptive significance of hybridization and introgression events, is
578
central to interpret and even predict the outcomes of these processes. Despite a few thoroughly
579
studied cases in other regions (Rieseberg et al., 2003), this is an elusive topic. Evidence in the
580
region is scanty but not lacking. For example, niche expansion associated with hybridization and
581
introgression is suggested in Armeria pungens (Piñeiro et al., 2011). Along with ecological
24
582
determinants of hybridization, a second crucial aspect is finely assessing reproductive barriers
583
between hybridizing species, which need not be constant across their ranges (e.g., in Narcissus,
584
Marques et al., 2012). The role of pollinators as premating barriers is very diverse. Examples of
585
week premating barriers involving pollinator sharing but leading to sterile hybrids due to post-
586
mating barriers include Mediterranean orchids (Cozzolino and Widmer, 2005). A third difficult
587
aspect is distinguishing introgression from lineage sorting (Albaladejo et al., 2005; Maureira-
588
Butler et al., 2008; Blanco-Pastor et al., 2012) and detecting old introgression. Next generation
589
sequencing techniques offer new possibilities for addressing those problems (Twyford and Ennos,
590
2012).
591
(f) Changes in reproductive systems
592
Intraspecific breeding system variation is a form of diversity. Thus, it is not unexpected that
593
it is well represented and, due to its lability and adaptive significance, to have changed several
594
times in a biodiversity hot-spot like the Mediterranean Basin. A number of phylogeographically
595
framed studies have identified changes in the reproductive system within this region, e.g., in
596
Mercurialis (Pannell et al., 2004), Ecbalium (Costich and Meagher, 1992), Hypochaeris (Ortíz et al.,
597
2007), Epipactis (Tranchida-Lombardo et al., 2011) or Erodium (Alarcón et al., 2011), among
598
others. In addition, it has long been known that annual life-forms are well represented in the
599
Mediterranean Basin (Raunkiaer, 1934). Since annuals are frequently associated with selfing
600
(Stebbins, 1970) and the shift from perennial outcrossing to annual selfing is considered to be
601
mostly irreversible (Barrett, 2013), the good representation of this life-cycle might be an indirect
602
indication of active breeding systems shifts.
603
There are a number of factors that are well represented in the Mediterranean region that
604
might be associated to breeding systems changes, e.g., human disturbance (Eckert et al., 2010),
605
environmental changes causing stress particularly in trailing edge populations (Levin, 2012),
606
threats of inbreeding in narrow habitats (Fiz-Palacios et al., 2010) or the occurrence of
25
607
biogeographic crossroads, such as the Strait of Gibraltar area, where populations of the same
608
species with different breeding systems accumulate following range shifts across this region
609
(Rodríguez-Sánchez et al., 2008). In contrast to these dynamic scenarios, breeding system shifts
610
are sometimes associated with relatively stable evolutionary scenarios in which differentiation
611
has been mainly due to genetic drift (e.g., Nigella in Bittkau and Comes, 2005; Comes et al., 2008).
612
Understanding the origin and maintenance of alternative reproductive systems is far from
613
simple and requires multiple approaches that go from the genetic basis to the ecological drivers
614
(Barrett, 1998; Charlesworth, 2006). However, breeding system variation revealed in a
615
phylogeographic context is a first step that can unveil possible associations between breeding
616
systems and haplotypes across space.
617
(g) Ecology determining success of colonization
618
Seedling establishment is a crucial stage in the colonization of new spots and, in general, in
619
species range expansion. When LDD events are involved, the success of colonization has been
620
traditionally been thought to depend primarily on the availability of dispersal vectors and other
621
factors related with the transport of the diaspores (Nathan, 2006) at least within historical
622
biogeography. This view somehow implies that once the most stochastic event is achieved, i.e.,
623
transporting a diaspore across a long distance, the rest of the elements for colonizing a new
624
territory are or comparatively minor importance. In recent years a view has emerged that gives a
625
bigger role in the colonization of new areas after LDD or surmounting narrow sea-barriers to
626
colonization abilities based on preadaptation of genotypes and availability of suitable habitats.
627
This view follows from research using different approaches including phylogeographically-
628
oriented studies from high latitudes (Alsos et al., 2007) and from Mediterranean groups. Among
629
the latter, some have stressed the lack of adaptations in seeds for transmarine transport
630
(Rodríguez-Sánchez et al., 2008; Fernández-Mazuecos and Vargas, 2010). Another study, using
631
species distribution modelling (SDM) and genetic data, has shown that the source of a successful
26
632
LDD of Armeria pungens from Iberia to Corsica-Sardinia were the populations occurring in the
633
most similar habitats, which happened to be geographically the most distant (Piñeiro et al., 2007).
634
If this pattern is frequent, it would be more correct to speak of long-distance colonization than of
635
long-distance dispersal, based on the idea that what we recognize as such are those events in
636
which colonization in the new territory has been achieved, whereas LDD events could be much
637
more frequent but many not resulting in successful colonization and therefore remaining
638
undetected.
639
640
IV. PERSPECTIVES
641
Plant phylogeography in the Mediterranean region will probably progress first by increasing the
642
number of markers sampled within genomes, as in any other discipline in evolutionary biology.
643
The main advantage of using genealogies from uniparentally inherited genes, i.e., discarding the
644
possibility of recombination and thus of mixed historical signals (Avise et al., 1987; Avise, 2009),
645
has been partly overridden years ago by the access to a range of multilocus markers such as
646
AFLPs, microsatellites, SNPs, and more recently by the availability of high throughput sequencing
647
techniques, even for non-model organisms (Emerson et al., 2010). This trend has been boosted by
648
the urge to sample larger parts of genomes when facing complex patterns and processes as we do
649
in the Mediterranean and also by the realization that relying on one or two gene genealogies to
650
infer past events at the species level, as done in classical phylogeography, entails risks. However,
651
inferring organism level evolution from that deluge of molecular data will continue to pose
652
problems that, conceptually, are not that different from those faced by molecular phylogenetics
653
in the nineties, i.e., homology/paralogy issues and the connections and disconnections between
654
gene tree and species tree.
655
A second aspect is the development and use of new approaches that seek to circumvent the
656
conceptual problems of more classical approaches. Knowles and Maddison (2002) introduced the
27
657
field of statistical phylogeography, which uses statistical approaches based on coalescent models
658
for parameter estimation and testing of alternative hypothesis. They focus on the processes that
659
generate the patterns of genetic variation and on assessing the confidence of phylogeographic
660
conclusions (Hickerson et al., 2010). The main argument is that if coalescent theory is not
661
considered, equating genealogical pattern with demographic and evolutionary processes may be
662
flawed (Arbogast et al., 2002). For example, genealogical splits caused by the same historical
663
abiotic event need not coincide exactly in time for two species showing disparate demographic
664
parameters (Knowles, 2009). Although several coalescent-based hypotheses testing methods
665
have been implemented, approximate Bayesian computation (ABC) is becoming increasingly used
666
since it bypasses the computational difficulties of calculating likelihood functions (Beaumont et
667
al., 2002). These methods are starting to be applied also in comparative phylogeographic studies
668
(Hierarchical Approximate Bayesian Computation methods, HABC). HABC methods estimate
669
‘hyper-parameters’, which inform degree of congruence among co-distributed species and ‘sub-
670
parameters’, which describe the demographic history of each species (Hickerson et al., 2006;
671
Beaumont, 2010). To the extent that statistical phylogeography minimizes the role of genealogies
672
(“a gene genealogy is a transitional variable for connecting data to demographic parameters
673
under an explicit statistical model” Hickerson et al., 2010), it is arguable whether it contributes to
674
narrowing the gap between phylogenetics and population genetics, as originally proposed by
675
Avise et al. (1987), and has led to hot debates (Beaumont et al., 2010). In any case, these
676
approaches should be tried in Mediterranean plant phylogeographic studies, where to date they
677
are virtually absent, unlike niche modelling approaches, which have been successfully used in
678
Mediterranean groups.
679
A third important component for the future of Mediterranean phylogeography is seeking for
680
congruence with independent data to improve the uncertainty and provide robustness to
681
phylogeographic hypotheses. Due to scantiness of the plant macrofossil record and the limited
682
utility of fossil pollen beyond non wind-pollinated species (Petit et al., 2002; Carrión et al., 2003;
28
683
López de Heredia et al., 2007; Terrab et al., 2008a), independent past evidence is expected to be
684
scarce for many plant groups. This is despite findings like those reported in Anderson et al. (2009)
685
in volcanic islands such as the Canaries, which remembers how fossil discovery is possible even in
686
places in which it was considered unlikely. Palaeoclimatic reconstructions in the Mediterranean
687
Basin and the projection of species distribution modelling into past scenarios (Waltari et al., 2007;
688
Benito-Garzón et al., 2007; Rodríguez-Sánchez and Arroyo, 2008; Rodríguez-Sánchez et al., 2010;
689
Fernández-Mazuecos and Vargas, 2013) are effective strategies to incorporate past evidence into
690
phylogeographic studies. But their usefulness will partly depend on filing gaps of palaeoclimatic
691
data for eastern and southern areas of the Basin and on refining them to be representative of the
692
environmental heterogeneity in the region (Jakob et al., 2007; Médail and Diadema, 2009).
693
Choosing simplified systems, e.g., with linear distribution ranges, may help in searching for
694
congruence too (Clausing et al., 2000; Piñeiro et al., 2007; Escudero et al., 2010).
695
Focusing on drivers of differentiation and thus beyond the neutral marker domain, another
696
interesting pursue is performing genome scans and searching for outlier loci showing a
697
significantly higher degree of differentiation, as this may be indicative of adaptive divergence
698
particularly when there is correlation with environmental variables (Herrera and Bazaga, 2008;
699
Excoffier et al., 2009; García et al., 2013). This exemplifies the tendency towards broadening the
700
scope of evolutionary questions addressed under a phylogeographic frame, which is likely to
701
increase as phylogeography becomes more inclusive. Combining efforts into integrative
702
hypothesis-based approaches is one of the keys to understand the complex picture of how the
703
Mediterranean biota have interacted and evolved along the Basin (Salvo et al., 2010).
704
Deepening comparative studies with the other four Mediterranean climate zones could also
705
throw light on plant evolution within the Basin (Cowling et al., 1996). Altogether the
706
Mediterranean biome covers 2% of the world’s surface, but is home to 20% of the total world’s
707
flora (Médail and Quézel, 1997). While some Mediterranean climate zones show common
708
features beyond the climate and the floristic richness, factors determining this richness and the
29
709
processes leading to it seem to differ substantially. For instance, the Mediterranean Basin seems
710
to share the high speciation and low extinction rates as well as the complex environmental
711
conditions with the Cape region and, maybe to some extent, the importance of soil types. Yet,
712
other factors that have apparently played a significant role in the diversity of the Cape region
713
were not crucial in the Mediterranean Basin. These are climatic stability (at least in comparable
714
terms), explosive radiation of a few clades that constitute most of the diversity, shifts in fire-
715
survival strategy, the timing of the onset of summer drought (Linder and Hardy, 2004; Linder,
716
2005; Schnitzler et al., 2011) and, underlying all these factors, lineage age (Valente and Vargas,
717
2013).
718
Large-scale comparative studies could also help to understand features of plant evolution in
719
time and space in this region. Large efforts like the IntraBiodiv Consortium that focused on the
720
Alps and Carpathians (e.g., Alvarez et al., 2009) would be useful in the Mediterranean but studies
721
focused on specific questions could give clues too. An example of the latter is Normand et al.
722
(2011), which assessed the relative importance of current climate vs. postglacial accessibility to
723
places with suitable conditions for explaining current plant species ranges in Europe. This study
724
found that accessibility was especially important for small-range species in southern Europe.
725
Another important question was addressed by the same team looking at the relationships
726
between Plio-Pleistocene climate changes, species richness and topographic heterogeneity. They
727
found a greater increase in species richness with increasing topographic heterogeneity in
728
southern Europe, than in northern Europe (Svenning et al., 2009).
729
In addition to the above exposed directions, some final remarks should be pointed out
730
regarding future phylogeographic studies in the Basin. There are substantial gaps in geographic
731
coverage for plant phylogeographic studies such as North Africa, the Balkans and the easternmost
732
part of the Basin. New evidence from the latter area is crucial to substantiate the idea that the
733
Eastern Mediterranean is a cradle for lineages diversification (Mansion et al., 2009; Barres et al.,
734
2013). Also, it is fortunate that recent rapid speciation events—associated with Pleistocene
30
735
climatic changes—have substantially contributed to the whole diversity of the area compared to
736
the Cape Flora (Valente and Vargas, 2013). Thus reconstructing the evolutionary history of a
737
growing number of younger lineages in the Mediterranean Basin, for which phylogeographic
738
approaches are particularly useful, will be insightful for the whole biota, including the possible
739
influence of humans. Because the location and dynamics of glacial refugia depend heavily on the
740
ecological requirements of each species, important questions regarding their role have to be
741
addressed using comparative approaches of species from the same habitats and with similar
742
biological characteristics.
743
All these things considered, the Mediterranean Basin continues to offer a highly
744
stimulating scientific ground which phylogeographic approaches can exploit with strong potential
745
to help explaining biodiversity patterns and understanding how the Basin has come to be one of
746
biodiversity hotspots on earth.
747
748
VI. ACKNOWLEDGEMENTS
749
I am grateful to Inés Álvarez, Elena Conti, Javier Fuertes, Myriam Heuertz, Joachim W. Kadereit,
750
Josep A. Rosselló, Isabel Sanmartín and two anonymous reviewers for providing very helpful
751
comments, and to Peter Linder for suggesting that I write this review, as well as for suggestions
752
and discussion. Support from the Spanish Ministerio de Ciencia e Innovación through the project
753
CGL2010-16138 is also acknowledged.
31
754
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FIGURE LEGENDS:
1346
Figure 1.- Delimitation of the Mediterranean region according to bioclimatic criteria (redrawn
1347
from Quézel and Médail, 2003)
1348
Figure 2.- Examples of east-west phylogeographic breaks associated with a distinct current
1349
geographic gap. Distribution ranges of Buxus balearica (red), Erophaca baetica (grey) and
1350
Cephalaria squamiflora (black) according to Rosselló et al. (2007), Casimiro-Soriguer et al., (2010)
1351
and Rosselló et al. (2009), respectively.
1352
Figure 3.- Examples of the refugia-within-refugia model advocating that each of the three
1353
southern European peninsulas did not function as a single refugium during Pleistocene glacial
1354
periods but each hosted different lineages in separate refugia as indicated by current genetic
1355
structure (Gomez and Lunt, 2007). The map gathers information from a different plant group in
1356
each of three peninsulas: hypothetic location of refugia during the LGM for Quercus spp. in the
1357
Iberian peninsula according to Olalde et al. (2002); genetic groups in Arabis alpina in the Italian
1358
peninsula (Ansell et al., 2008); taxonomic-genetic groups in the Cardamine maritima complex in
1359
the Balkans (Kučera et al., 2010).
1360
Figure 4.- Sea straits whose biogeographic role as barriers or corridors has been addressed in
1361
phylogeographic studies around the Mediterranean Basin.
1362
Figure 5.- Examples of inferred long-distance dispersal (LDD) events within the Mediterranean
1363
Basin in Androsace vitaliana (dark blue), Papaver alpinum (yellow), Cheirolophus intybaceus (red),
1364
Armeria pungens (lilac), Juniperus thurifera (light blue), Anthemis secundirramea (green), Linaria
1365
Sect. Versicolores (orange), interpreted from Dixon et al. (2009), Kropf et al. (2006), Garnatje et al.
1366
(2012), Piñeiro et al. (2007), Terrab et al. (2008b), Lo Presti and Oberprieler (2011) and
1367
Fernández-Mazuecos and Vargas (2011), respectively.
56